Advertisement

Journal of Ethology

, Volume 30, Issue 2, pp 247–254 | Cite as

Male-biased sex ratio increases female egg laying and fitness in the housefly, Musca domestica

  • Juli Carrillo
  • Anne Danielson-François
  • Evan Siemann
  • Lisa Meffert
Article

Abstract

A biased operational sex ratio (OSR) can have multiple, confounding effects on reproductive fitness. A biased OSR can increase harassment and mating activity directed towards potential mates but may also increase the ability of potential mates to choose a good partner if lower quality mates are screened out through competitive interactions. Additionally, a biased OSR may affect reproductive fitness through changes in male ejaculate content or in female reproductive response. We quantified how a male-biased OSR (1:1, 2:1, or 5:1 male to female) affected the size of a female’s first egg clutch and her offspring’s survivorship in the housefly, Musca domestica. A male-biased OSR increased female fitness: females laid more eggs in their first clutch, had increased offspring survivorship at a 2:1 versus 1:1 OSR, and had equivalent fitness with a 5:1 male to female OSR. Courtship activity increased when the OSR was male-biased but was not a significant predictor of female fitness. Trials where females chose their mates versus trials where a random male was chosen for them had equivalent first clutch sizes and offspring survivorship. These results suggest that there are cryptic effects from a male-biased OSR on female fitness that are most likely driven by pre-copulatory social environment.

Keywords

Competition Courtship Sex ratio OSR Sexual conflict Indirect effects Clutch size 

Notes

Acknowledgments

J.A.C. received support from an Alliance for Graduate Education and the Professoriate Research Fellowship (National Science Foundation Cooperative Agreement HRD-0450363), the Ford Foundation, and a National Science Foundation pre-doctoral fellowship. This work was supported by National Science Foundation DEB-0128855 to L.M. We would like to thank four anonymous reviewers for their insightful comments. All experiments complied with the current laws of the country in which they were performed.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Alonso-Pimentel H, Papaj DR (1996) Operational sex ratio versus gender density as determinants of copulation duration in the walnut fly, Rhagoletis juglandis (Diptera: Tephritidae). Behav Ecol Sociobiol 39:171–180CrossRefGoogle Scholar
  2. Andres JA, Arnqvist G (2001) Genetic divergence of the seminal signal-receptor system in houseflies: the footprints of sexually antagonistic coevolution? Proc R Soc Lond B 268:399–405CrossRefGoogle Scholar
  3. Arnqvist G, Andres JA (2006) The effects of experimentally induced polyandry on female reproduction in a monandrous mating system. Ethology 112:748–756CrossRefGoogle Scholar
  4. Arnqvist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60:145–164PubMedCrossRefGoogle Scholar
  5. Avancini RMP, Silveira GAR (2000) Age structure and abundance in populations of muscoid flies from a poultry facility in Southeast Brazil. Mem Inst Oswaldo Cruz 95:259–264PubMedCrossRefGoogle Scholar
  6. Avila FW, Sirot LK, LaFlamme BA, Rubinstein CD, Wolfner MF (2011) Insect seminal fluid proteins: identification and function. Annu Rev Entomol 56:21–40PubMedCrossRefGoogle Scholar
  7. Berglund A (1994) The operational sex-ratio influences choosiness in a pipefish. Behav Ecol 5:254–258CrossRefGoogle Scholar
  8. Bisazza A, Marconato A (1988) Female mate choice, male-male competition and parental care in the river bullhead, Cottus gobio L. (Pisces, Cottidae). Anim Behav 36:1352–1360CrossRefGoogle Scholar
  9. Bryant EH (1969) Fates of immatures in mixtures of 2 housefly strains. Ecology 50:1049–1069CrossRefGoogle Scholar
  10. Bretman A, Fricke C, Chapman T (2009) Plastic responses of male Drosophila melanogaster to the level of sperm competition increase male reproductive fitness. Proc R Soc Lond B 276:1705–1711CrossRefGoogle Scholar
  11. Cakir S, Kence A (2000) Polymorphism of M factors in populations of the housefly, Musca domestica L., in Turkey. Genet Res 76:19–25PubMedCrossRefGoogle Scholar
  12. Cameron E, Day T, Rowe L (2003) Sexual conflict and indirect benefits. J Evol Biol 16:1055–1060PubMedCrossRefGoogle Scholar
  13. Cordoba-Aguilar A (2009) A female evolutionary response when survival is at risk: male harassment mediates early reallocation of resources to increase egg number and size. Behav Ecol Sociobiol 63:751–763CrossRefGoogle Scholar
  14. Emlen ST, Oring LW (1977) Ecology, sexual selection, and evolution of mating systems. Science 197:215–223PubMedCrossRefGoogle Scholar
  15. Fedorka KM, Winterhalter WE, Ware B (2011) Perceived sperm competition intensity influences seminal fluid protein production prior to courtship and mating. Evolution 65:584–590PubMedCrossRefGoogle Scholar
  16. Feldmeyer B, Kozielska M, Kuijper B, Weissing FJ, Beukeboom LW, Pen I (2008) Climatic variation and the geographical distribution of sex-determining mechanisms in the housefly. Evol Ecol Res 10:797–809Google Scholar
  17. Friberg U, Arnqvist G (2003) Fitness effects of female mate choice: preferred males are detrimental for Drosophila melanogaster females. J Evol Biol 16:797–811PubMedCrossRefGoogle Scholar
  18. Gavrilets S, Arnqvist G, Friberg U (2001) The evolution of female mate choice by sexual conflict. Proc R Soc Lond B 268:531–539CrossRefGoogle Scholar
  19. Grant JWA, Foam PE (2002) Effect of operational sex ratio on female–female versus male–male competitive aggression. Can J Zool Rev 80:2242–2246CrossRefGoogle Scholar
  20. Head ML, Brooks R (2006) Sexual coercion and the opportunity for sexual selection in guppies. Anim Behav 71:515–522CrossRefGoogle Scholar
  21. Heubel KU, Lindstrom K, Kokko H (2008) Females increase current reproductive effort when future access to males is uncertain. Biol Lett 4:224–227PubMedCrossRefGoogle Scholar
  22. Hicks SK, Hagenbuch KL, Meffert LM (2004) Variable costs of mating, longevity, and starvation resistance in Musca domestica (Diptera: Muscidae). Environ Entomol 33:779–786CrossRefGoogle Scholar
  23. Holland B, Rice WR (1999) Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes a reproductive load. Proc Natl Acad Sci USA 96:5083–5088PubMedCrossRefGoogle Scholar
  24. Hosken D, Ward P (2001) Experimental evidence for testis size evolution via sperm competition. Ecol Lett 4:10–13CrossRefGoogle Scholar
  25. Jirotkul M (1999) Operational sex ratio influences female preference and male-male competition in guppies. Anim Behav 58:287–294PubMedCrossRefGoogle Scholar
  26. Kvarnemo C, Forsgren E, Magnhagen C (1995) Effects of sex ratio on intra- and inter-sexual behaviour in sand gobies. Anim Behav 50:1455–1461CrossRefGoogle Scholar
  27. Lauer MJ, Sih A, Krupa JJ (1996) Male density, female density and inter-sexual conflict in a stream-dwelling insect. Anim Behav 52:929–939CrossRefGoogle Scholar
  28. Lemaître J-F, Ramm SA, Hurst JL, Stockley P (2010) Social cues of sperm competition influence accessory reproductive gland size in a promiscuous mammal. Proc R Soc Lond B 278:1171–1176CrossRefGoogle Scholar
  29. Leopold RA (1976) The role of male accessory glands in insect reproduction. Annu Rev Entomol 21:199–221CrossRefGoogle Scholar
  30. Meffert LM, Bryant EH (1991) Mating propensity and courtship behavior in serially bottlenecked lines of the housefly. Evolution 45:293–306CrossRefGoogle Scholar
  31. Meffert LM, Hagenbuch KL (2005) The genetic architecture of house fly mating behavior. In: Current topics in developmental biology, vol 66. Elsevier, San Diego, pp 189–213Google Scholar
  32. Meffert LM, Hicks SK, Regan JL (2002) Nonadditive genetic effects in animal behavior. Am Nat 160:S198–S213PubMedCrossRefGoogle Scholar
  33. Meffert LM, Regan JL (2002) A test of speciation via sexual selection on female preferences. Anim Behav 64:955–965CrossRefGoogle Scholar
  34. Meffert LM, Regan JL, Brown BW (1999) Convergent evolution of the mating behaviour of founder-flush populations of the housefly. J Evol Biol 12:859–868CrossRefGoogle Scholar
  35. Ojanguren AF, Magurran AE (2007) Male harassment reduces short-term female fitness in guppies. Behaviour 144:503–514CrossRefGoogle Scholar
  36. Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567Google Scholar
  37. Parker GA (1979) Sexual selection and sexual conflict. In: Blum MS, Blum NA (eds) Sexual selection and reproductive competition in insects. Academic, New York, pp 123–166Google Scholar
  38. Parker GA (2006) Sexual conflict over mating and fertilization: an overview. Philos Trans R Soc Lond B 361:235–259CrossRefGoogle Scholar
  39. Prohl H (2002) Population differences in female resource abundance, adult sex ratio, and male mating success in Dendrobates pumilio. Behav Ecol 13:175–181CrossRefGoogle Scholar
  40. Pound N, Gage MJG (2004) Prudent sperm allocation in Norway rats, Rattus norvegicus: a mammalian model of adaptive ejaculate adjustment. Anim Behav 68:819–823CrossRefGoogle Scholar
  41. Ragland SS, Sohal RS (1973) Mating behavior, physical activity and aging in housefly, Musca-domestica. Exp Gerontol 8:135–145PubMedCrossRefGoogle Scholar
  42. Reed DH, Bryant EH (2004) Phenotypic correlations among fitness and its components in a population of the housefly. J Evol Biol 17:919–923PubMedCrossRefGoogle Scholar
  43. Reichard M, Jurajda P, Smith C (2004) Male-male interference competition decreases spawning rate in the European bitterling (Rhodeus sericeus). Behav Ecol Sociobiol 56:34–41CrossRefGoogle Scholar
  44. Riemann JG, Thorson BJ (1969) Effect of male accessory material on oviposition and mating by female house flies. Ann Entomol Soc Am 62:828–834PubMedGoogle Scholar
  45. Riemann JG, Moen DJ, Thorson BJ (1967) Female monogamy and its control in houseflies. Insect Physiol 13:407–418CrossRefGoogle Scholar
  46. Ros AFH, Zeilstra I, Oliveira RF (2003) Mate choice in the Galilee St. Peter’s fish, Sarotherodon galilaeus. Behaviour 140:1173–1188CrossRefGoogle Scholar
  47. Sakurai G, Kasuya E (2008) The costs of harassment in the adzuki bean beetle. Anim Behav 75:1367–1373CrossRefGoogle Scholar
  48. Simmons LW (2001) Sperm competition and its evolutionary consequences in the insects. Princeton University Press, PrincetonGoogle Scholar
  49. Simmons LW, Denholm A, Jackson C, Levy E, Madon E (2007) Male crickets adjust ejaculate quality with both risk and intensity of sperm competition. Biol Lett 3:520–522PubMedCrossRefGoogle Scholar
  50. Stockley P (1997) Sexual conflict resulting from adaptations to sperm competition. Trends Ecol Evol 12:154–159PubMedCrossRefGoogle Scholar
  51. Tomita T, Wada Y (1989) Multifactorial sex determination in natural-populations of the housefly (Musca-Domestica) in Japan. Jpn J Genet 64:373–382CrossRefGoogle Scholar
  52. Weir LK, Grant JWA, Hutchings JA (2011) The influence of operational sex ratio on the intensity of competition for mates. Am Nat 177:167–176PubMedCrossRefGoogle Scholar
  53. Wigby S, Sirot LK, Linklater JR, Buehner N, Calboli FCF, Bretman A, Wolfner MF, Chapman T (2009) Seminal fluid protein allocation and male reproductive success. Curr Biol 19:751–757PubMedCrossRefGoogle Scholar
  54. Wolfner MF (2002) The gifts that keep on giving: physiological functions and evolutionary dynamics of male seminal proteins in Drosophila. Heredity 88:85–93Google Scholar

Copyright information

© Japan Ethological Society and Springer 2011

Authors and Affiliations

  • Juli Carrillo
    • 1
  • Anne Danielson-François
    • 1
    • 2
  • Evan Siemann
    • 1
  • Lisa Meffert
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyRice UniversityHoustonUSA
  2. 2.Division of Biology, Department of Natural SciencesUniversity of Michigan-DearbornDearbornUSA

Personalised recommendations